Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni

Anne E Lockyer, Aidan M Emery, Richard A Kane, Anthony J Walker, Claus D Mayer, Guillaume Mitta, Christine Coustau, Coen M Adema, Ben Hanelt, David Rollinson, Leslie R Noble, Catherine S Jones

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Abstract

The outcome of infection in the host snail Biomphalaria glabrata with the digenean parasite Schistosoma mansoni is determined by the initial molecular interplay occurring between them. The mechanisms by which schistosomes evade snail immune recognition to ensure survival are not fully understood, but one possibility is that the snail internal defence system is manipulated by the schistosome enabling the parasite to establish infection. This study provides novel insights into the nature of schistosome resistance and susceptibility in B. glabrata at the transcriptomic level by simultaneously comparing gene expression in haemocytes from parasite-exposed and control groups of both schistosome-resistant and schistosome-susceptible strains, 2 h post exposure to S. mansoni miracidia, using an novel 5 K cDNA microarray. Differences in gene expression, including those for immune/stress response, signal transduction and matrix/adhesion genes were identified between the two snail strains and tests for asymmetric distributions of gene function also identified immune-related gene expression in resistant snails, but not in susceptible. Gene set enrichment analysis revealed that genes involved in mitochondrial electron transport, ubiquinone biosynthesis and electron carrier activity were consistently up-regulated in resistant snails but down-regulated in susceptible. This supports the hypothesis that schistosome-resistant snails recognize schistosomes and mount an appropriate defence response, while in schistosome-susceptible snails the parasite suppresses this defence response, early in infection.

Original languageEnglish
Article numbere51102
Number of pages16
JournalPloS ONE
Volume7
Issue number12
DOIs
Publication statusPublished - 26 Dec 2012

Keywords

  • microarray data
  • primary sporocysts
  • defense cells
  • intermediate snail host
  • system
  • compatability
  • infection
  • echinostoma-paraensei
  • discovery
  • superoxide-dismutase

Cite this

Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni. / Lockyer, Anne E; Emery, Aidan M; Kane, Richard A; Walker, Anthony J; Mayer, Claus D; Mitta, Guillaume; Coustau, Christine; Adema, Coen M; Hanelt, Ben; Rollinson, David; Noble, Leslie R; Jones, Catherine S.

In: PloS ONE, Vol. 7, No. 12, e51102, 26.12.2012.

Research output: Contribution to journalArticle

Lockyer, Anne E ; Emery, Aidan M ; Kane, Richard A ; Walker, Anthony J ; Mayer, Claus D ; Mitta, Guillaume ; Coustau, Christine ; Adema, Coen M ; Hanelt, Ben ; Rollinson, David ; Noble, Leslie R ; Jones, Catherine S. / Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni. In: PloS ONE. 2012 ; Vol. 7, No. 12.
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abstract = "The outcome of infection in the host snail Biomphalaria glabrata with the digenean parasite Schistosoma mansoni is determined by the initial molecular interplay occurring between them. The mechanisms by which schistosomes evade snail immune recognition to ensure survival are not fully understood, but one possibility is that the snail internal defence system is manipulated by the schistosome enabling the parasite to establish infection. This study provides novel insights into the nature of schistosome resistance and susceptibility in B. glabrata at the transcriptomic level by simultaneously comparing gene expression in haemocytes from parasite-exposed and control groups of both schistosome-resistant and schistosome-susceptible strains, 2 h post exposure to S. mansoni miracidia, using an novel 5 K cDNA microarray. Differences in gene expression, including those for immune/stress response, signal transduction and matrix/adhesion genes were identified between the two snail strains and tests for asymmetric distributions of gene function also identified immune-related gene expression in resistant snails, but not in susceptible. Gene set enrichment analysis revealed that genes involved in mitochondrial electron transport, ubiquinone biosynthesis and electron carrier activity were consistently up-regulated in resistant snails but down-regulated in susceptible. This supports the hypothesis that schistosome-resistant snails recognize schistosomes and mount an appropriate defence response, while in schistosome-susceptible snails the parasite suppresses this defence response, early in infection.",
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note = "Acknowledgments We would like to thank Jayne King and Mike Anderson, NHM, for snail and parasite culture, and Julia Llewellyn-Hughes and Steve Llewellyn Hughes for using the Microlab Star robotic work station (Hamilton) to pick the clones. Microarrays were printed at the Department of Pathology, Cambridge University, by Anthony Brown.",
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T1 - Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni

AU - Lockyer, Anne E

AU - Emery, Aidan M

AU - Kane, Richard A

AU - Walker, Anthony J

AU - Mayer, Claus D

AU - Mitta, Guillaume

AU - Coustau, Christine

AU - Adema, Coen M

AU - Hanelt, Ben

AU - Rollinson, David

AU - Noble, Leslie R

AU - Jones, Catherine S

N1 - Acknowledgments We would like to thank Jayne King and Mike Anderson, NHM, for snail and parasite culture, and Julia Llewellyn-Hughes and Steve Llewellyn Hughes for using the Microlab Star robotic work station (Hamilton) to pick the clones. Microarrays were printed at the Department of Pathology, Cambridge University, by Anthony Brown.

PY - 2012/12/26

Y1 - 2012/12/26

N2 - The outcome of infection in the host snail Biomphalaria glabrata with the digenean parasite Schistosoma mansoni is determined by the initial molecular interplay occurring between them. The mechanisms by which schistosomes evade snail immune recognition to ensure survival are not fully understood, but one possibility is that the snail internal defence system is manipulated by the schistosome enabling the parasite to establish infection. This study provides novel insights into the nature of schistosome resistance and susceptibility in B. glabrata at the transcriptomic level by simultaneously comparing gene expression in haemocytes from parasite-exposed and control groups of both schistosome-resistant and schistosome-susceptible strains, 2 h post exposure to S. mansoni miracidia, using an novel 5 K cDNA microarray. Differences in gene expression, including those for immune/stress response, signal transduction and matrix/adhesion genes were identified between the two snail strains and tests for asymmetric distributions of gene function also identified immune-related gene expression in resistant snails, but not in susceptible. Gene set enrichment analysis revealed that genes involved in mitochondrial electron transport, ubiquinone biosynthesis and electron carrier activity were consistently up-regulated in resistant snails but down-regulated in susceptible. This supports the hypothesis that schistosome-resistant snails recognize schistosomes and mount an appropriate defence response, while in schistosome-susceptible snails the parasite suppresses this defence response, early in infection.

AB - The outcome of infection in the host snail Biomphalaria glabrata with the digenean parasite Schistosoma mansoni is determined by the initial molecular interplay occurring between them. The mechanisms by which schistosomes evade snail immune recognition to ensure survival are not fully understood, but one possibility is that the snail internal defence system is manipulated by the schistosome enabling the parasite to establish infection. This study provides novel insights into the nature of schistosome resistance and susceptibility in B. glabrata at the transcriptomic level by simultaneously comparing gene expression in haemocytes from parasite-exposed and control groups of both schistosome-resistant and schistosome-susceptible strains, 2 h post exposure to S. mansoni miracidia, using an novel 5 K cDNA microarray. Differences in gene expression, including those for immune/stress response, signal transduction and matrix/adhesion genes were identified between the two snail strains and tests for asymmetric distributions of gene function also identified immune-related gene expression in resistant snails, but not in susceptible. Gene set enrichment analysis revealed that genes involved in mitochondrial electron transport, ubiquinone biosynthesis and electron carrier activity were consistently up-regulated in resistant snails but down-regulated in susceptible. This supports the hypothesis that schistosome-resistant snails recognize schistosomes and mount an appropriate defence response, while in schistosome-susceptible snails the parasite suppresses this defence response, early in infection.

KW - microarray data

KW - primary sporocysts

KW - defense cells

KW - intermediate snail host

KW - system

KW - compatability

KW - infection

KW - echinostoma-paraensei

KW - discovery

KW - superoxide-dismutase

U2 - 10.1371/journal.pone.0051102

DO - 10.1371/journal.pone.0051102

M3 - Article

VL - 7

JO - PloS ONE

JF - PloS ONE

SN - 1932-6203

IS - 12

M1 - e51102

ER -